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The response of breeding pairs of Mongolian gerbils to intruders
BEHAVIORALAND NEURALBIOLOGY32, 516--523 (1981)
BRIEF REPORT The Response of Breeding Pairs of Mongolian Gerbils to Intruders ELLEN R. STOCKMAN *A AND MELINDA A. NOVAK*'t *Zoology and tPsychology Departments, University of Massachusetts, Amherst, Massachusetts 01003 Male and female Mongolian gerbils, Meriones unguiculatus, are known to be aggressive toward unfamiliar conspecifics introduced into their home territories. A longitudinal study of three mated pairs of gerbils was conducted to determine the effect of the female's reproductive state upon the pair's reactions toward male and female intruders. Pairs were observed during 10-min tests with individual male and female intruders and in the absence of an intruder during several pregnancies and lactation periods. Several nonsocial behaviors were depressed in the presence, as compared to the absence, of an intruder. Affiliative and agonistic contacts between mates increased in the presence of an intruder, and agonistic contact between mates was higher in the presence of a male intruder than a female. No other effects of intruder sex were observed. Virtually all contacts between residents and intruders were aggressive and sexual interactions were never observed. The reproductive condition of the female resident had no effect upon their aggressiveness or that of their mates toward intruders. Time spent by females in the nest increased and contact between mates decreased during the lactation period.
On the steppes of central Asia, Mongolian gerbils (Meriones unguiculatus) occur at densities as high as 70 to 176 per hectare, and up to 26 gerbils have been found in a single burrow (Naumov & Lobachev, 1975). Social interactions among these animals are presumably frequent, but observations of the social behavior of this species in its natural habitat have not yet been gathered. Under laboratory or seminatural conditions, Mongolian gerbils cohabit amicably as mated pairs or in familiar groups. They are, however, intolerant of unfamiliar conspecifics, and severe fighting occurs when intruders enter the home cages or pens of resident animals. If the conTo whom requests for reprints should be sent at: Department of Physiology and Biophysics, Howard University College of Medicine, 520 W St., N.W., Washington, D.C. 20059. We wish to acknowledge with thanks the assistance provided by Dr. Jerrold Meyer. 516 0163 - 1047/81/080516-08 $02.00/0 Copyright @ 1981 by AcademicPress, Inc. All rightsof reproductionin any form reserved.
RESPONSE OF GERBILS TO INTRUDERS
517
frontation occurs in a small cage, the intruder may suffer severe injury unless the session is terminated quickly (Nyby, Thiessen, & Wallace, 1970). In large enclosures, both male and female gerbils defend their territory against unfamiliar animals of both sexes (Agren, 1976). We have attempted to extend these findings by investigating the role of the female resident's reproductive state upon the behavior of resident pairs toward intruders introduced into their home pen. In other laboratory rodent species, female aggressiveness toward intruders is much higher during the lactation period than at other times (Svare & Gandelman, 1976, and others). We wanted to determine whether a postpartum increase in aggression could be observed in gerbils under seminatural conditions and whether it would influence the behavior of a mated pair toward intruders. Intruders of both sexes were used because intruder sex has been shown to affect the behavior of resident animals in the gerbil (Agren & Meyerson, 1977) and other rodent species (Alberts & Galef, 1973; DeBold & Miczek, 1979). A longitudinal design, in which three resident pairs were studied across several reproductive cycles, was chosen in an effort to keep conditions as natural as possible. We wished to avoid the frequent removal and handling which are necessary to accurately determine reproductive state, and we also wanted to avoid too-frequent testing. Our design enabled us to introduce intruders only three times a week and yet counterbalance intruder sex and order of observation of subjects within each reproductive state. Three multiparous pairs of gerbils from our laboratory colony were employed as resident animals. Each pair was housed in a 2-m 2 pen filled with a sand and soil mixture to a depth of approximately 7 cm. Food, water, and bedding material were provided and open, wire-mesh cages were placed in the center and corners of each pen to provide a refuge for the intruders. A 14-hr light-dark cycle was maintained and all data were gathered during the last 5 hr of the light period. The resident animals were allowed to habituate to their pens for 2 weeks before testing began. The intruders were 70- to 100-day-old male and female gerbils that were housed from weaning in single-sex groups. Data were collected on the behavior of the resident animals during sessions with male and female intruders and during control sessions when no intruder was present. By noting the dates of parturition, it was possible to determine the reproductive state of the female residents during each session. Sufficient data for analysis were obtained during three reproductive states of the resident females--midpregnancy (8-14 days before birth), late pregnancy (1-7 days before birth), and postpartum (Days 0-6 postpartum, litter present). It was not possible to obtain sufficient data during other reproductive states because postpartum impregnation often
518
STOCKMAN AND NOVAK
confounded the mid- to late lactation period with early pregnancy. Each pair produced four or five litters during the 6 months of study, but copulatory behavior was never observed during an experimental session. The resident pairs were observed as follows. At the beginning of each of three weekly experimental sessions, a male or female intruder was dropped into a corner of the pen and allowed to remain in the pen for 10 min. The observer, using a focal subject procedure, recorded the behavior of the male and female resident for 5 min each. Intruders were used only once per resident pair. One to three control sessions, in which the resident pairs were observed in the absence of an intruder, were run each week. Behavior was recorded using a modified frequency scoring system in which the 10-rain observation period was subdivided into 40 15-sec intervals. The modified frequency refers to the number of intervals in which the behavior occurred. Eleven categories of behavior were measured. Noncontact behavior included: total alert (a combination of upright, locomote, and sniff), footstomping (drumming with the hind legs), digging, ingesting, gnawing lying down, and in nest. Contact behavior included: contact young (primarily exhibited by females), affiliative contact with mate (including groom, and nasal or body contact), agonistic contact with mate, and agonistic contact with intruder. Agonistic contact included fighting, attacking, chasing, and threatening. Threaten was scored whenever the resident exhibited a sidling posture toward the intruder (Roper & Polioudakis, 1977) or whenever the resident's attack was blocked by one of the wire-mesh cages. Data were gathered during 36 sessions per resident pair, representing 12 sessions per reproductive state. Of each 12, four were gathered in the presence of a male intruder, four in the presence of a female intruder, and four with no intruder present. These were completely counterbalanced for order of observation of residents. These data were subjected to a four-way mixed design analysis of variance with resident sex, female's reproductive state, and intruder condition as main effects and sessions as a repeated measure. Significant treatment effects were further analyzed with the Newman-Keuls post hoc text (Newman, 1939). The ANOVA was chosen because we were interested in possible interactions between our variables. Time-dependent behavioral changes were assessed using three-way ANOVAs performed on the data from the first 8 weeks of the experiment. The level of significance for all analyses was set at p < .01. Consistent with previous reports (Agren, 1976) the resident gerbils were highly aggressive toward the intruders. The intruders were always submissive and frequently crawled under a wire-mesh cage when threatened by a resident. After the second or third encounter, male residents
519
RESPONSE OF GERBILS TO INTRUDERS
consistently initiated aggression within 30 sec of intruder introduction. Female residents were more variable, sometimes attacking immediately and, at other times, retreating and avoiding confrontation. Both the nonsocial behaviors of resident gerbils and their social interactions with each other were affected by the presence of an intruder. As can be seen in Fig. 1, resident animals exhibited less digging (F(2, 8) = 14.92, p < .005), gnawing (F(2, 8) = 12.12, p < .005), and lying down (F(2, 8) = 10.15, p < .01) when an intruder was present and more affiliative contact (F(2, 8) = 21.58, p < .005) with each other (see Fig. 2). Lactating female residents tended to spend less time in contact with their young when an intruder was present, although this effect was not significant. Also, in the presence of an intruder, as compared to the absence of an intruder, residents exhibited more agonistic behavior toward one another (F(2, 8) = 68.22, p < .005). As Fig. 2 shows, the presence of a male intruder resulted in a greater increase in agonistic behavior between mates than did the presence of a female. Post hoc analysis revealed that this was a significant difference. No other effect of intruder sex was found. Residents were equally aggressive to male and female intruders, and no sexual interactions were observed between residents and intruders. 15, FNI - FEMALE RESIDENT, NO INTRUDER PRESENT FI - FEMALE RESIDENT, INTRUDER PRESENT >tJ Z u.I ::) 0 uJ
MNI - MALE RESIDENT, NO INTRUDER PRESENT
12'
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FIG. 1. L e v e l s of four noncontact behaviors exhibited by male and female resident gerbils in the presence or absence of an intruder as a function of the resident female's reproductive state.
520
STOCKMAN AND NOVAK 15' A-MALE INTRUDER PRESENT >. 12.
A-FEMALE INTRUOER PRESENT
Z UJ
O-NO INTRUDER PRESENT
o UJ 0 UJ rr,
o Z ILl
E
-~
AFFILIATIVE CONTACT WITH MATE
E AGONISTIC CONTACT WITH MATE
FIG. 2. L e v e l s o f affiliative a n d agonistic contact b e t w e e n residents exhibited in the presence of a male intruder, a female intruder, or no intruder as a function o f the resident f e m a l e ' s reproductive state.
The pattern of agonistic response exhibited by female residents did not vary across the three reproductive conditions studies, nor did that of their mates (F(2, 8) = .98, not significant) (see Fig. 3). Other behaviors were affected by reproductive state. Females spent more time in the nest (F(2, 8) = 18.80, p < .005) and residents engaged in less affiliative contact (F(2, 8) = 12.75, p < .005) when young were present (see Figs. 1 and 2). Consistent sex differences in the behavior of the resident animals included lower levels of lying down (F(1, 4) = 21.33, p < .01) and contact young (F(1, 4) = 121.11, p < .005) and higher levels of total alert (F(2, 8) = 11.88, p < .005) and footstomping (F(2, 8) = 21.26, p < .005) in male as opposed to female residents. Male residents were more aggressive toward intruders than were females, and this effect approached significance (F(2, 4) = 14.97, p < .025). Scent-marking behavior was exhibited by both male and female residents, but its incidence was too low for analysis. Two behaviors showed time-related effects. Total alert increased over time under all intruder conditions (F(7, 28) = 3.42, p < .01) and on all
RESPONSE OF GERBILS TO INTRUDERS
MALE >- 12 Z t,u
0 uJ u. 9 C=
521
RESIDENTS
~
O'~INTRUDER PRESENT
INTRUDER PRESENT
_.u
CI 0
FEMALE RESIDENTS 6
z
~
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O ' ~ I N T RUDER PRESENT
~N I TRUDERPRESE.T
0
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AGONISTIC CONTACT WITH INTRUDER
FIc. 3. Levels of agonistic contact by male and female resident gerbils directed toward male or female intruders as a function of the resident female's reproductive state.
fours increased during sessions with an intruder present (F(7, 28) = 3.64, p < .01). We were, at first, surprised that our female residents failed to show a postpartum increase in aggression, as this effect has been observed in other rodent species. Svare and Gandelman (1976) found that mice tested during six successive reproductive cycles showed an increase in aggression during the lactation phase, as compared to the pregnant phase, of each cycle. In all of these studies, however, females were tested in the absence of their mates. In a recent study, DeBold and Miczek (1979) introduced intruders into small mixed-sex colonies of rats, and no correlation was found between aggression and female residents' reproductive condition (pregnant or lactating). Their findings, combined with our own, suggest that, in some species, a postpartum increase in aggression toward intruders is not apparent when females are tested in the presence of familiar males. Deer mice may differ from rats and gerbils in this regard (Ayer & Whitsett, 1980). Our failure to observe differences in the behaviors of resident gerbils directed at male, as opposed to female, intruders, was quite unexpected. We were particularly surprised that male residents were as consistently aggressive toward females as they were to males. In DeBold and Miczek's (1979) study, patterns of aggression were sex specific. Residents were
522
STOCKMAN AND NOVAK
intensely aggressive to intruders of their own sex, but seldom attacked those of the opposite sex. Other investigators have observed some aggression both by male gerbils (Agren, 1976; Agren & Meyerson, 1977) and by male rats (Alberts & Galef, 1973) directed at unfamiliar females, but in these studies sexual, as well as aggressive, behaviors were frequently observed. It is possible that some aspect of our apparatus or procedure predisposed the male residents toward aggressive, as opposed to sexual responses toward female intruders. An increase in fighting among resident gerbils, like that observed in response to intruders in the present study, was reported by Agren (1976). A differential increase in fighting in response to male versus female intruders, however, has not been previously reported in this species. This finding is particularly interesting because it represents the only effect of intruder sex observed in the present study. Poole and Morgan (1975) reported a similar difference in intragroup aggression when male and female intruders were introduced into a colony of mice. Our conclusions may be summarized as follows: (I) Under some conditions, female gerbils fail to show a postpartum increase in aggression toward intruders. (2) Resident gerbils respond differentially to the presence of a male, as opposed to a female intruder. This differential response is evident in the levels of aggression observed between mates, but not in their aggression toward the intruders. (3) Like other mammalian species, gerbils show consistent sex differences in behaviors related to aggression and parental care.
REFERENCES Agren, G. (1976). Social and territorial behavior in the Mongolian gerbil (Meriones unguiculatus) under seminatural conditions. Biology of Behavior, 1, 267-285. Agren, G., & Meyerson, B. J. (1977). Influence of gonadal hormones and social housing conditions on agonistic, copulatory, and related sociosexual behavior in the Mongolian gerbil (Meriones unguiculatus). Behavioral Processes, 2, 265-282. Alberts, J. R., & Galef, B. G. (1973). Olfactory cues and movement: Stimuli mediating intraspecific aggression in the wild Norway rat. Journal of Comparative and Physiological Psychology, 85, 233-242. Ayer, M. L., & Whitsett, J. M. (1980). Aggressive behavior of female prairie deer mice in laboratory populations. Animal Behavior, 28, 763-771. DeBold, J. F., & Miczek, K. A. (1979). Aggressive behavior is dependent on gonadal steroids in male but not female rats. Society for Neuroscience Abstracts, 5, 442. Naumov, N. P., & Lobachev, V. S. (1975). Ecology of the desert rodents of the U.S.S.R. (Jerboas and Gerbils). In I. Prakash & P. K. Ghosh (Eds.), Rodents in Desert Environments, pp. 530-536. The Hague: Junk. Newman, D. (1939). The distribution of range in samples from a normal population expressed in terms of an independent estimate of standard deviation. Biometrika, 31, 20-30. Nyby, J., Thiessen, D. D., & Wallace, P. (1970). Social inhibition of territorial marking in the Mongolian gerbil (Meriones unguiculatus). Psychonomic Science, 21~ 310-312. Poole, T. B., & Morgan, H. D. R. (1975). Aggressive behavior of male mice (Mus musculus) toward familiar and unfamiliar opponents. Animal Behavior, 23, 470-479.
RESPONSE OF GERBILS TO INTRUDERS
523
Roper, T. J., & Polioudakis, E. (1977). The behavior of Mongolian gerbils in a semi-natural environment, with special reference to ventral marking, dominance and sociability. Behavior, 61, 207-237. Schwentker, V. (1963). The gerbil--A new laboratory animal. Illinois Veterinarian, 6, 5-9. Svare, B., & Gandelman, R. (1976). A longitudinal analysis of maternal aggression in Rockland-Swiss albino mice. Developmental Psychobiology, 9, 437-446.
BRIEF REPORT The Response of Breeding Pairs of Mongolian Gerbils to Intruders ELLEN R. STOCKMAN *A AND MELINDA A. NOVAK*'t *Zoology and tPsychology Departments, University of Massachusetts, Amherst, Massachusetts 01003 Male and female Mongolian gerbils, Meriones unguiculatus, are known to be aggressive toward unfamiliar conspecifics introduced into their home territories. A longitudinal study of three mated pairs of gerbils was conducted to determine the effect of the female's reproductive state upon the pair's reactions toward male and female intruders. Pairs were observed during 10-min tests with individual male and female intruders and in the absence of an intruder during several pregnancies and lactation periods. Several nonsocial behaviors were depressed in the presence, as compared to the absence, of an intruder. Affiliative and agonistic contacts between mates increased in the presence of an intruder, and agonistic contact between mates was higher in the presence of a male intruder than a female. No other effects of intruder sex were observed. Virtually all contacts between residents and intruders were aggressive and sexual interactions were never observed. The reproductive condition of the female resident had no effect upon their aggressiveness or that of their mates toward intruders. Time spent by females in the nest increased and contact between mates decreased during the lactation period.
On the steppes of central Asia, Mongolian gerbils (Meriones unguiculatus) occur at densities as high as 70 to 176 per hectare, and up to 26 gerbils have been found in a single burrow (Naumov & Lobachev, 1975). Social interactions among these animals are presumably frequent, but observations of the social behavior of this species in its natural habitat have not yet been gathered. Under laboratory or seminatural conditions, Mongolian gerbils cohabit amicably as mated pairs or in familiar groups. They are, however, intolerant of unfamiliar conspecifics, and severe fighting occurs when intruders enter the home cages or pens of resident animals. If the conTo whom requests for reprints should be sent at: Department of Physiology and Biophysics, Howard University College of Medicine, 520 W St., N.W., Washington, D.C. 20059. We wish to acknowledge with thanks the assistance provided by Dr. Jerrold Meyer. 516 0163 - 1047/81/080516-08 $02.00/0 Copyright @ 1981 by AcademicPress, Inc. All rightsof reproductionin any form reserved.
RESPONSE OF GERBILS TO INTRUDERS
517
frontation occurs in a small cage, the intruder may suffer severe injury unless the session is terminated quickly (Nyby, Thiessen, & Wallace, 1970). In large enclosures, both male and female gerbils defend their territory against unfamiliar animals of both sexes (Agren, 1976). We have attempted to extend these findings by investigating the role of the female resident's reproductive state upon the behavior of resident pairs toward intruders introduced into their home pen. In other laboratory rodent species, female aggressiveness toward intruders is much higher during the lactation period than at other times (Svare & Gandelman, 1976, and others). We wanted to determine whether a postpartum increase in aggression could be observed in gerbils under seminatural conditions and whether it would influence the behavior of a mated pair toward intruders. Intruders of both sexes were used because intruder sex has been shown to affect the behavior of resident animals in the gerbil (Agren & Meyerson, 1977) and other rodent species (Alberts & Galef, 1973; DeBold & Miczek, 1979). A longitudinal design, in which three resident pairs were studied across several reproductive cycles, was chosen in an effort to keep conditions as natural as possible. We wished to avoid the frequent removal and handling which are necessary to accurately determine reproductive state, and we also wanted to avoid too-frequent testing. Our design enabled us to introduce intruders only three times a week and yet counterbalance intruder sex and order of observation of subjects within each reproductive state. Three multiparous pairs of gerbils from our laboratory colony were employed as resident animals. Each pair was housed in a 2-m 2 pen filled with a sand and soil mixture to a depth of approximately 7 cm. Food, water, and bedding material were provided and open, wire-mesh cages were placed in the center and corners of each pen to provide a refuge for the intruders. A 14-hr light-dark cycle was maintained and all data were gathered during the last 5 hr of the light period. The resident animals were allowed to habituate to their pens for 2 weeks before testing began. The intruders were 70- to 100-day-old male and female gerbils that were housed from weaning in single-sex groups. Data were collected on the behavior of the resident animals during sessions with male and female intruders and during control sessions when no intruder was present. By noting the dates of parturition, it was possible to determine the reproductive state of the female residents during each session. Sufficient data for analysis were obtained during three reproductive states of the resident females--midpregnancy (8-14 days before birth), late pregnancy (1-7 days before birth), and postpartum (Days 0-6 postpartum, litter present). It was not possible to obtain sufficient data during other reproductive states because postpartum impregnation often
518
STOCKMAN AND NOVAK
confounded the mid- to late lactation period with early pregnancy. Each pair produced four or five litters during the 6 months of study, but copulatory behavior was never observed during an experimental session. The resident pairs were observed as follows. At the beginning of each of three weekly experimental sessions, a male or female intruder was dropped into a corner of the pen and allowed to remain in the pen for 10 min. The observer, using a focal subject procedure, recorded the behavior of the male and female resident for 5 min each. Intruders were used only once per resident pair. One to three control sessions, in which the resident pairs were observed in the absence of an intruder, were run each week. Behavior was recorded using a modified frequency scoring system in which the 10-rain observation period was subdivided into 40 15-sec intervals. The modified frequency refers to the number of intervals in which the behavior occurred. Eleven categories of behavior were measured. Noncontact behavior included: total alert (a combination of upright, locomote, and sniff), footstomping (drumming with the hind legs), digging, ingesting, gnawing lying down, and in nest. Contact behavior included: contact young (primarily exhibited by females), affiliative contact with mate (including groom, and nasal or body contact), agonistic contact with mate, and agonistic contact with intruder. Agonistic contact included fighting, attacking, chasing, and threatening. Threaten was scored whenever the resident exhibited a sidling posture toward the intruder (Roper & Polioudakis, 1977) or whenever the resident's attack was blocked by one of the wire-mesh cages. Data were gathered during 36 sessions per resident pair, representing 12 sessions per reproductive state. Of each 12, four were gathered in the presence of a male intruder, four in the presence of a female intruder, and four with no intruder present. These were completely counterbalanced for order of observation of residents. These data were subjected to a four-way mixed design analysis of variance with resident sex, female's reproductive state, and intruder condition as main effects and sessions as a repeated measure. Significant treatment effects were further analyzed with the Newman-Keuls post hoc text (Newman, 1939). The ANOVA was chosen because we were interested in possible interactions between our variables. Time-dependent behavioral changes were assessed using three-way ANOVAs performed on the data from the first 8 weeks of the experiment. The level of significance for all analyses was set at p < .01. Consistent with previous reports (Agren, 1976) the resident gerbils were highly aggressive toward the intruders. The intruders were always submissive and frequently crawled under a wire-mesh cage when threatened by a resident. After the second or third encounter, male residents
519
RESPONSE OF GERBILS TO INTRUDERS
consistently initiated aggression within 30 sec of intruder introduction. Female residents were more variable, sometimes attacking immediately and, at other times, retreating and avoiding confrontation. Both the nonsocial behaviors of resident gerbils and their social interactions with each other were affected by the presence of an intruder. As can be seen in Fig. 1, resident animals exhibited less digging (F(2, 8) = 14.92, p < .005), gnawing (F(2, 8) = 12.12, p < .005), and lying down (F(2, 8) = 10.15, p < .01) when an intruder was present and more affiliative contact (F(2, 8) = 21.58, p < .005) with each other (see Fig. 2). Lactating female residents tended to spend less time in contact with their young when an intruder was present, although this effect was not significant. Also, in the presence of an intruder, as compared to the absence of an intruder, residents exhibited more agonistic behavior toward one another (F(2, 8) = 68.22, p < .005). As Fig. 2 shows, the presence of a male intruder resulted in a greater increase in agonistic behavior between mates than did the presence of a female. Post hoc analysis revealed that this was a significant difference. No other effect of intruder sex was found. Residents were equally aggressive to male and female intruders, and no sexual interactions were observed between residents and intruders. 15, FNI - FEMALE RESIDENT, NO INTRUDER PRESENT FI - FEMALE RESIDENT, INTRUDER PRESENT >tJ Z u.I ::) 0 uJ
MNI - MALE RESIDENT, NO INTRUDER PRESENT
12'
OFNI I
I I
e~ i/J m
I I
ii.
/FI
o o
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MI - MALE RESIDENT, INTRUDER PRESENT
/
/
I I
6"
%
/
% \
/
z
//
/
3
O/
I
%(~MNI
-,:,
~
IN NEST ~
~.
/ F I
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~
®
LIE DOWN ~
~-
.a
.e
DIG
&
n'
0 ''~
L ~ ' - - - ~'OFNI A ~F[4M
=
®
~
o
GNAW "
FIG. 1. L e v e l s of four noncontact behaviors exhibited by male and female resident gerbils in the presence or absence of an intruder as a function of the resident female's reproductive state.
520
STOCKMAN AND NOVAK 15' A-MALE INTRUDER PRESENT >. 12.
A-FEMALE INTRUOER PRESENT
Z UJ
O-NO INTRUDER PRESENT
o UJ 0 UJ rr,
o Z ILl
E
-~
AFFILIATIVE CONTACT WITH MATE
E AGONISTIC CONTACT WITH MATE
FIG. 2. L e v e l s o f affiliative a n d agonistic contact b e t w e e n residents exhibited in the presence of a male intruder, a female intruder, or no intruder as a function o f the resident f e m a l e ' s reproductive state.
The pattern of agonistic response exhibited by female residents did not vary across the three reproductive conditions studies, nor did that of their mates (F(2, 8) = .98, not significant) (see Fig. 3). Other behaviors were affected by reproductive state. Females spent more time in the nest (F(2, 8) = 18.80, p < .005) and residents engaged in less affiliative contact (F(2, 8) = 12.75, p < .005) when young were present (see Figs. 1 and 2). Consistent sex differences in the behavior of the resident animals included lower levels of lying down (F(1, 4) = 21.33, p < .01) and contact young (F(1, 4) = 121.11, p < .005) and higher levels of total alert (F(2, 8) = 11.88, p < .005) and footstomping (F(2, 8) = 21.26, p < .005) in male as opposed to female residents. Male residents were more aggressive toward intruders than were females, and this effect approached significance (F(2, 4) = 14.97, p < .025). Scent-marking behavior was exhibited by both male and female residents, but its incidence was too low for analysis. Two behaviors showed time-related effects. Total alert increased over time under all intruder conditions (F(7, 28) = 3.42, p < .01) and on all
RESPONSE OF GERBILS TO INTRUDERS
MALE >- 12 Z t,u
0 uJ u. 9 C=
521
RESIDENTS
~
O'~INTRUDER PRESENT
INTRUDER PRESENT
_.u
CI 0
FEMALE RESIDENTS 6
z
~
s i ' J ~ '~ ,~.
O ' ~ I N T RUDER PRESENT
~N I TRUDERPRESE.T
0
m
n.
AGONISTIC CONTACT WITH INTRUDER
FIc. 3. Levels of agonistic contact by male and female resident gerbils directed toward male or female intruders as a function of the resident female's reproductive state.
fours increased during sessions with an intruder present (F(7, 28) = 3.64, p < .01). We were, at first, surprised that our female residents failed to show a postpartum increase in aggression, as this effect has been observed in other rodent species. Svare and Gandelman (1976) found that mice tested during six successive reproductive cycles showed an increase in aggression during the lactation phase, as compared to the pregnant phase, of each cycle. In all of these studies, however, females were tested in the absence of their mates. In a recent study, DeBold and Miczek (1979) introduced intruders into small mixed-sex colonies of rats, and no correlation was found between aggression and female residents' reproductive condition (pregnant or lactating). Their findings, combined with our own, suggest that, in some species, a postpartum increase in aggression toward intruders is not apparent when females are tested in the presence of familiar males. Deer mice may differ from rats and gerbils in this regard (Ayer & Whitsett, 1980). Our failure to observe differences in the behaviors of resident gerbils directed at male, as opposed to female, intruders, was quite unexpected. We were particularly surprised that male residents were as consistently aggressive toward females as they were to males. In DeBold and Miczek's (1979) study, patterns of aggression were sex specific. Residents were
522
STOCKMAN AND NOVAK
intensely aggressive to intruders of their own sex, but seldom attacked those of the opposite sex. Other investigators have observed some aggression both by male gerbils (Agren, 1976; Agren & Meyerson, 1977) and by male rats (Alberts & Galef, 1973) directed at unfamiliar females, but in these studies sexual, as well as aggressive, behaviors were frequently observed. It is possible that some aspect of our apparatus or procedure predisposed the male residents toward aggressive, as opposed to sexual responses toward female intruders. An increase in fighting among resident gerbils, like that observed in response to intruders in the present study, was reported by Agren (1976). A differential increase in fighting in response to male versus female intruders, however, has not been previously reported in this species. This finding is particularly interesting because it represents the only effect of intruder sex observed in the present study. Poole and Morgan (1975) reported a similar difference in intragroup aggression when male and female intruders were introduced into a colony of mice. Our conclusions may be summarized as follows: (I) Under some conditions, female gerbils fail to show a postpartum increase in aggression toward intruders. (2) Resident gerbils respond differentially to the presence of a male, as opposed to a female intruder. This differential response is evident in the levels of aggression observed between mates, but not in their aggression toward the intruders. (3) Like other mammalian species, gerbils show consistent sex differences in behaviors related to aggression and parental care.
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Roper, T. J., & Polioudakis, E. (1977). The behavior of Mongolian gerbils in a semi-natural environment, with special reference to ventral marking, dominance and sociability. Behavior, 61, 207-237. Schwentker, V. (1963). The gerbil--A new laboratory animal. Illinois Veterinarian, 6, 5-9. Svare, B., & Gandelman, R. (1976). A longitudinal analysis of maternal aggression in Rockland-Swiss albino mice. Developmental Psychobiology, 9, 437-446.